Mechanisms underlying interferon-γ-induced priming of microglial reactive oxygen species production

PLoS ONE

Volumn 11, Issue 9, 2016, Pages

  Spencer, Nicholas G ^a   Schilling, Tom ^a   Miralles, Francesc ^a   Eder, Claudia ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENOSINE TRIPHOSPHATE; CYSTEINE; GAMMA INTERFERON; GLUTATHIONE; GLYCOPROTEIN GP 91; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; MITOGEN ACTIVATED PROTEIN KINASE P38; N ACETYL LEVO CYSTEINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; 2-(2-METHYL-1H-INDOL-3-YL)-1H-IMIDAZOL(4,5-F)(1,10)PHENANTHROLINE; ACETYLCYSTEINE; CYBB PROTEIN, MOUSE; ENZYME INHIBITOR; GLYCOPROTEIN; GP91DS-TAT PROTEIN, CHIMERIC; IMIDAZOLE DERIVATIVE; INDUCIBLE NITRIC OXIDE SYNTHASE; INWARDLY RECTIFYING POTASSIUM CHANNEL; MEMBRANE PROTEIN; NOS2 PROTEIN, MOUSE; PEROXYNITROUS ACID; PHENANTHROLINE DERIVATIVE; PYRIDINE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; CELL LEVEL; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MICROGLIA; PROTEIN EXPRESSION; UPREGULATION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; SIGNAL TRANSDUCTION;

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; GLUTATHIONE; GLYCOPROTEINS; IMIDAZOLES; INTERFERON-GAMMA; MEMBRANE GLYCOPROTEINS; MICE; MICROGLIA; NADPH OXIDASE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEROXYNITROUS ACID; PHENANTHROLINES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PYRIDINES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84992327130     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0162497     Document Type: Article

References (46)

1. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007; 8: 57-69. PMID: 17180163
2. Nayernia Z, Jaquet V, Krause KH. New insights on NOX enzymes in the central nervous system. Antioxid Redox Signal. 2014; 20: 2815-2837. doi: 10.1089/ars.2013.5703 PMID: 24206089
3. Zhang J, Wang X, Vikash V, Ye Q, Wu D, Liu Y, et al. ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev. 2016; 2016: 4350965. doi: 10.1155/2016/4350965 PMID: 26998193
4. Rojo AI, McBean G, Cindric M, Egea J, López MG, Rada P, et al. Redox control of microglial function: molecular mechanisms and functional significance. Antioxid Redox Signal. 2014; 21: 1766-1801. doi: 10.1089/ars.2013.5745 PMID: 24597893
5. Haslund-Vinding J, McBean G, Jaquet V, Vilhardt F. NADPH oxidases in microglia oxidant production: activating receptors, pharmacology, and association with disease. Br J Pharmacol. 2016; doi: 10.1111/bph.13425. [Epub ahead of print].
6. Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, Posmantur R. P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem. 2003; 278: 13309-13317. PMID: 12551918
7. El-Benna J, Dang PM, Gougerot-Pocidalo MA. Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin Immunopathol. 2008; 30: 279-289. doi: 10.1007/s00281-008-0118-3 PMID: 18536919
8. Van Muiswinkel FL, Veerhuis R, Eikelenboom P. Amyloid beta protein primes cultured rat microglial cells for an enhanced phorbol 12-myristate 13-acetate-induced respiratory burst activity. J Neurochem. 1996; 66: 2468-2476. PMID: 8632171
9. Klegeris A, McGeer PL. beta-amyloid protein enhances macrophage production of oxygen free radicals and glutamate. J Neurosci Res. 1997; 49: 229-235. PMID: 9272645
10. Schilling T, Eder C. Amyloid-ß-induced reactive oxygen species production and priming are differentially regulated by ion channels in microglia. J Cell Physiol. 2011; 226: 3295-3302. doi: 10.1002/jcp. 22675 PMID: 21321937
11. Chao CC, Hu S, Peterson PK. Modulation of human microglial cell superoxide production by cytokines. J Leukoc Biol. 1995; 58: 65-70. PMID: 7616108
12. Hu S, Sheng WS, Peterson PK, Chao CC. Cytokine modulation of murine microglial cell superoxide production. Glia. 1995; 13: 45-50. PMID: 7751055
13. Vilhardt F, Plastre O, Sawada M, Suzuki K, Wiznerowicz M, Kiyokawa E, et al. The HIV-1 Nef protein and phagocyte NADPH oxidase activation. J Biol Chem. 2002; 277: 42136-42143. PMID: 12207012
14. Purisai MG, McCormack AL, Cumine S, Li J, Isla MZ, Di Monte DA. Microglial activation as a priming event leading to paraquat-induced dopaminergic cell degeneration. Neurobiol Dis. 2007; 25: 392-400. PMID: 17166727
15. Hallett MB, Lloyds D. Neutrophil priming: the cellular signals that say 'amber' but not 'green'. Immunol Today. 1995; 16: 264-268. PMID: 7662095
16. Perry VH, Holmes C. Microglial priming in neurodegenerative disease. Nat Rev Neurol. 2014; 10: 217-224. doi: 10.1038/nrneurol.2014.38 PMID: 24638131
17. Norden DM, Muccigrosso MM, Godbout JP. Microglial priming and enhanced reactivity to secondary insult in aging, and traumatic CNS injury, and neurodegenerative disease. Neuropharmacology. 2015; 96: 29-41. doi: 10.1016/j.neuropharm.2014.10.028 PMID: 25445485
18. Minogue AM, Jones RS, Kelly RJ, McDonald CL, Connor TJ, Lynch MA. Age-associated dysregulation of microglial activation is coupled with enhanced blood-brain barrier permeability and pathology in APP/PS1 mice. Neurobiol Aging. 2014; 35: 1442-1452. doi: 10.1016/j.neurobiolaging.2013.12.026 PMID: 24439957
19. Ansari MA. Temporal profile of M1 and M2 responses in the hippocampus following early 24h of neurotrauma. J Neurol Sci. 2015; 357: 41-49. doi: 10.1016/j.jns.2015.06.062 PMID: 26148932
20. McManus RM, Higgins SC, Mills KH, Lynch MA. Respiratory infection promotes T cell infiltration and amyloid-ß deposition in APP/PS1 mice. Neurobiol Aging. 2014; 35: 109-121. doi: 10.1016/j. neurobiolaging.2013.07.025 PMID: 23993702
21. Mangano EN, Litteljohn D, So R, Nelson E, Peters S, Bethune C, et al. Interferon-γ plays a role in paraquat-induced neurodegeneration involving oxidative and proinflammatory pathways. Neurobiol Aging. 2012; 33: 1411-1426. doi: 10.1016/j.neurobiolaging.2011.02.016 PMID: 21482445
22. Schmitz M, Hermann P, Oikonomou P, Stoeck K, Ebert E, Poliakova T, et al. Cytokine profiles and the role of cellular prion protein in patients with vascular dementia and vascular encephalopathy. Neurobiol Aging. 2015; 36: 2597-2606. doi: 10.1016/j.neurobiolaging.2015.05.013 PMID: 26170132
23. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. Immortalization of murine microglial cells by a vraf/v-myc carrying retrovirus. J Neuroimmunol. 1990; 27: 229-237. PMID: 2110186
24. Eder C. Ion channels in monocytes and microglia/brain macrophages: promising therapeutic targets for neurological diseases. J Neuroimmunol. 2010; 224: 51-55. doi: 10.1016/j.jneuroim.2010.05.008 PMID: 20554024
25. Lowry OH, Passonneau JV, Hasselberger FX, Schulz DW. Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain. J Biol Chem. 1964; 239: 18-30. PMID: 14114842
26. Beis I, Newsholme EA. The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. Biochem J. 1975; 152: 23-32. PMID: 1212224
27. Schilling T, Miralles F, Eder C. TRPM7 regulates proliferation and polarisation of macrophages. J Cell Sci. 2014; 127: 4561-4566. doi: 10.1242/jcs.151068 PMID: 25205764
28. Njie EG, Boelen E, Stassen FR, Steinbusch HW, Borchelt DR, Streit WJ. Ex vivo cultures of microglia from young and aged rodent brain reveal age-related changes in microglial function. Neurobiol Aging. 2012; 33: 195.e1-12.
29. Steinert JR, Chernova T, Forsythe ID. Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist. 2010; 16: 435-452. doi: 10.1177/1073858410366481 PMID: 20817920
30. Bhattacharya A, Biber K. The microglial ATP-gated ion channel P2X7 as a CNS drug target. Glia. 2016; 64: 1772-1787. doi: 10.1002/glia.23001 PMID: 27219534
31. Dale E, Staal RG, Eder C, Möller T. KCa3.1-a microglial target ready for drug repurposing? Glia. 2016; 64: 1733-1741. doi: 10.1002/glia.22992 PMID: 27121595
32. Khanna R, Roy L, Zhu X, Schlichter LC. K+ channels and the microglial respiratory burst. Am J Physiol Cell Physiol. 2001; 280: C796-C806. PMID: 11245596
33. Thomas MP, Chartrand K, Reynolds A, Vitvitsky V, Banerjee R, Gendelman HE. Ion channel blockade attenuates aggregated alpha synuclein induction of microglial reactive oxygen species: relevance for the pathogenesis of Parkinson's disease. J Neurochem. 2007; 100: 503-519. PMID: 17241161
34. Milton RH, Abeti R, Averaimo S, DeBiasi S, Vitellaro L, Jiang L, et al. CLIC1 function is required for ß-amyloid-induced generation of reactive oxygen species by microglia. J Neurosci. 2008; 28: 11488-11499. doi: 10.1523/JNEUROSCI.2431-08.2008 PMID: 18987185
35. Schilling T, Eder C. Importance of the non-selective cation channel TRPV1 for microglial reactive oxygen species generation. J Neuroimmunol. 2009; 216: 118-121. doi: 10.1016/j.jneuroim.2009.07.008 PMID: 19683814
36. Schilling T, Eder C. Stimulus-dependent requirement of ion channels for microglial NADPH oxidasemediated production of reactive oxygen species. J Neuroimmunol. 2010; 225: 190-194. doi: 10.1016/j. jneuroim.2010.05.024 PMID: 20554029
37. Wu LJ, Wu G, Akhavan Sharif MR, Baker A, Jia Y, Fahey FH, et al. The voltage-gated proton channel Hv1 enhances brain damage from ischemic stroke. Nat Neurosci. 2012; 15: 565-573. doi: 10.1038/nn. 3059 PMID: 22388960
38. Kettenmann H, Hoppe D, Gottmann K, Banati R, Kreutzberg G. Cultured microglial cells have a distinct pattern of membrane channels different from peritoneal macrophages. J Neurosci Res. 1990; 26: 278-287. PMID: 1697905
39. McLarnon JG, Xu R, Lee YB, Kim SU. Ion channels of human microglia in culture. Neuroscience. 1997; 78: 1217-1228. PMID: 9174088
40. Schilling T, Eder C. Microglial K+ channel expression in young adult and aged mice. Glia. 2015; 63: 664-672. doi: 10.1002/glia.22776 PMID: 25472417
41. Franciosi S, Choi HB, Kim SU, McLarnon JG. Interferon-γ acutely induces calcium influx in human microglia. J Neurosci Res. 2002; 69: 607-613. PMID: 12210826
42. Park YC, Jun CD, Kang HS, Kim HD, Kim HM, Chung HT. Role of intracellular calcium as a priming signal for the induction of nitric oxide synthesis in murine peritoneal macrophages. Immunology. 1996; 87: 296-302. PMID: 8698394
43. Nair JS, DaFonseca CJ, Tjernberg A, Sun W, Darnell JE Jr, Chait BT, et al. Requirement of Ca2+ and CaMKII for Stat1 Ser-727 phosphorylation in response to IFN-gamma. Proc Natl Acad Sci U S A. 2002; 99: 5971-5976. PMID: 11972023
44. Lam D, Schlichter LC. Expression and contributions of the Kir2.1 inward-rectifier K+ channel to proliferation, migration and chemotaxis of microglia in unstimulated and anti-inflammatory states. Front Cell Neurosci. 2015; 9: 185. doi: 10.3389/fncel.2015.00185 PMID: 26029054
45. Surace MJ, Block ML. Targeting microglia-mediated neurotoxicity: the potential of NOX2 inhibitors. Cell Mol Life Sci. 2012; 69: 2409-2427. doi: 10.1007/s00018-012-1015-4 PMID: 22581365
46. Diebold BA, Smith SM, Li Y, Lambeth JD. NOX2 as a target for drug development: indications, possible complications, and progress. Antioxid Redox Signal. 2015; 23: 375-405. doi: 10.1089/ars.2014.5862 PMID: 24512192